Most organisms belonging to the Saccharomycotina subphylum have high genetic diversity and a vast repertoire of metabolisms and lifestyles, which explains its ecological versatility. The yeast Lachancea cidri is an ideal model for exploring the interplay between genetics, ecological function and evolution. L. cidri is a species that diverged from the Saccharomyces lineage before the whole-genome duplication and exhibits a broad distribution across the South Hemisphere, thus displaying an important ecological success. Here, we applied phylogenomics to investigate the adaptive genetic variation of L. cidri isolates obtained from natural environments in Australia and South America. Our approach revealed the presence of two main lineages according to their geographic distribution (Aus and SoAm). Estimation of the divergence time suggest that South American and Australian lineages diverged near the last glacial maximum event during the Pleistocene (64-8 KYA), consistent with the presence of multiple glacial refugia. Interestingly, we found that the French reference strain belongs to the Australian lineage, with a recent divergence (405-51 YA), likely associated to human movements. Additionally, species delimitation analysis identified different evolutionary units within the South American lineage and, together with parameters like Pi (π) and FST, revealed that Patagonia contains most of the genetic diversity of this species. These results agree with phenotypic characterizations, demonstrating a greater phenotypic diversity in the South American lineage. These findings support the idea of a Pleistocene-dated divergence between South Hemisphere lineages, where the Nothofagus and Araucaria ecological niches likely favored the extensive distribution of L. cidri in Patagonia.